Desiccation tolerance in Anopheles coluzzii: the effects of spiracle size and cuticular hydrocarbons.

Arthur C Arcaz,Moussa Diallo,Diana L Huestis,John Andersen,Adama Dao,Gary J Blomquist,Tovi Lehmann,Alpha S Yaro

doi:10.1242/jeb.135665

Abstract

ABSTRACTThe African malaria mosquitoes Anopheles gambiae and Anopheles coluzzii range over forests and arid areas, where they withstand dry spells and months-long dry seasons, suggesting variation in their desiccation tolerance. We subjected a laboratory colony (G3) and wild Sahelian mosquitoes during the rainy and dry seasons to desiccation assays. The thoracic spiracles and amount and composition of cuticular hydrocarbons (CHCs) of individual mosquitoes were measured to determine the effects of these traits on desiccation tolerance. The relative humidity of the assay, body water available, rate of water loss and water content at death accounted for 88% of the variation in desiccation tolerance. Spiracle size did not affect the rate of water loss or desiccation tolerance of the colony mosquitoes, as was the case for the total CHCs. However, six CHCs accounted for 71% of the variation in desiccation tolerance and three accounted for 72% of the variation in the rate of water loss. Wild A. coluzzii exhibited elevated desiccation tolerance during the dry season. During that time, relative thorax and spiracle sizes were smaller than during the rainy season. A smaller spiracle size appeared to increase A. coluzzii's desiccation tolerance, but was not statistically significant. Seasonal changes in CHC composition were detected in Sahelian A. coluzzii. Stepwise regression models suggested the effect of particular CHCs on desiccation tolerance. In conclusion, the combination of particular CHCs along with the total amount of CHCs is a primary mechanism conferring desiccation tolerance in A. coluzzii, while variation in spiracle size might be a secondary mechanism.

Highlights

The importance of Anopheles gambiae and Anopheles coluzzii in the transmission of malaria is widely recognized (WHO, 2014), yet despite extensive research, major gaps remain in our understanding of fundamental aspects of their biology
We focused on the large metathoracic and mesothoracic spiracles, which vary in length (Nagpal et al, 2003; Wagoner et al, 2014), yet this variation has not been examined in terms of its effect on desiccation tolerance (DT)
Laboratory experiment DT and body water content Mosquitoes subjected to the desiccation assay survived longer in the high humidity treatment: 36.2 versus 16.3 h (P

Summary

INTRODUCTION

The importance of Anopheles gambiae and Anopheles coluzzii ( previously the S and M forms of A. gambiae, respectively) in the transmission of malaria is widely recognized (WHO, 2014), yet despite extensive research, major gaps remain in our understanding of fundamental aspects of their biology The ranges of these vectors cover steamy forests, dry savannas and semi-arid areas in Africa, 1Laboratory of Malaria and Vector Research, NIAID, NIH, Rockville, MD 20852, USA. We focused on the large metathoracic and mesothoracic spiracles, which vary in length (Nagpal et al, 2003; Wagoner et al, 2014), yet this variation has not been examined in terms of its effect on DT Mosquitoes close their spiracles presumably to optimize the balance between gas exchange and water loss (Gray and Bradley, 2006) based on external and internal factors, such as relative humidity (RH), hydration and starvation status (Chown and Nicolson, 2004; Krafsur, 1971). The order of these predictions follows our conceptual scheme, the laboratory experiment offers greater control over key parameters and it is treated earlier in the Results section

MATERIALS AND METHODS

RESULTS

DISCUSSION